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Bulletin of Insectology 63 (1): 59-63, 2010 ISSN 1721-8861

Detection of ‘Candidatus mali’ in different populations of melanoneura in Italy

1 1 1 1 1 Valeria MALAGNINI , Federico PEDRAZZOLI , Valeria GUALANDRI , Rosaly ZASSO , Elisa BOZZA , Federica 1 2 2 1 FIAMINGO , Alberto POZZEBON , Nicola MORI , Claudio IORIATTI 1Centro Trasferimento Tecnologico, FEM- IASMA, San Michele all’Adige, Trento, Italy 2Department of Environmental Agronomy and Crop Science, University of Padua, Legnaro, Padova, Italy

Abstract

Cacospylla melanoneura Förster ( ) is one of the vectors of ‘Candidatus Phytoplasma mali’, which is the causal agent of proliferation (AP) disease. In 2006 and 2007, overwintering adult psyllids were collected from different host plants (apple, hawthorn and conifers) in different localities to assess the natural infection of C. melanoneura. AP phytoplasma was detected in through the use of PCR amplification with specific primers (AP3/AP4). Eleven percent of the psyllids collected from apple in the Trentino region were infected with AP phytoplasma, as compared with 18.63% of the psyllids collected from apple in the Aosta Valley and none of the psyllids collected from apple in the Veneto region. The percentage of AP-positive overwintering adults was higher in the Aosta Valley than in the Trentino region. Furthermore, considering the level of AP pres- ence in the monitored orchards, a positive correlation between the infection rates in the insects and the percentage of symptomatic plants was observed. Regarding psyllids collected from hawthorn, only few individuals tested positive in Trentino populations, while higher infection levels were found out in the Aosta Valley. Interesting percentages of positive psyllids resulted also in the insects collected from conifers (10.5%). Data obtained in this work demonstrate therefore that ‘Ca. P. mali’ may overwinter in the body of C. melanoneura and that there are differences in the infection proportion among populations.

Key words: apple proliferation, phytoplasma, psyllids, , host plants.

Introduction emerged with C. melanoneura, with only one successful transmission out of 278 test plants (transmission rate of The agronomic importance of the Hemiptera genus Ca- 0.36%) (Mattedi et al., 2008). copsylla is linked to the role played by several species Despite the incidence of ‘Ca. P. mali’-infected apple as vectors of phytoplasma-associated diseases. Apple plants in all the apple growing areas of Trentino, the proliferation (AP) disease is one of the most severe abundance of both species is dramatically decreasing in problems in Italian apple (Malus domestica Borkh.) or- the last years. Interesting population levels are only pre- chards. In northeastern Italy, symptoms of AP have sent for C. melanoneura in Valsugana, while C. picta been observed since the 1950s (Rui, 1950), but the dis- density has drastically dropped down in the whole re- ease has only recently become widespread, particularly gion and therefore this study focuses on the role of the in Trentino (northeastern Italy), where it has struck the first species in AP epidemiology. cultivars Golden Delicious, Florina and Renetta Canada The biology of C. melanoneura in the apple orchards (Vindimian and Delaiti, 1996). AP causes important of Trentino has been studied in detail (Mattedi et al., economic losses, as infected trees produce small fruits 2007; 2008). Overwintering adults migrate into apple with poor flavour. orchards between the end of January and February. The aetiological agent, ‘Candidatus Phytoplasma Oviposition begins between the end of February and the mali’ (Seemüller and Schneider, 2004), is transmitted beginning of March and this activity lasts about 30-40 by two psyllids, with different efficiencies: Cacopsylla days. The first nymphs appear at the end of March and picta (Förster) is the main vector in north-eastern Italy the new generation of adults emerges at the end of (Carraro et al., 2001b) and C. melanoneura (Förster) in April. As the adults develop, they migrate to other shel- north-western Italy (Tedeschi et al., 2002). Studies con- ter plants and disappear from the orchard before the end ducted in Germany confirm the role of C. picta in the of June. epidemiology of AP disease, excluding the latter species During the same period, C. melanoneura can also be (Jarausch B. et al., 2004; Mayer et al., 2009). Both spe- found on hawthorn ( Jacq. and C. cies are present in Trentino, but with different distribu- oxyacantha L.) (Ossiannilsson, 1992), on which high tions: C. melanoneura is ubiquist and shows the highest population densities have been reported even in some population densities in bottom valley environments locations of Trentino (Pedrazzoli et al., 2005). Recently, (Adige Valley and Valsugana); the presence of C. picta experiments conducted in north-western Italy found that is limited to hilly areas, such as Non and Sole Valley C. melanoneura individuals collected from hawthorn (Mattedi et al., 2008). Transmission experiments with carried AP-group (Tedeschi et al., 2005; the two psyllids were therefore conducted also in this 2009). region over a six-years period (Mattedi et al., 2008). Besides hawthorn and apple, C. melanoneura has also Owing to these trials, the role of C. picta was confirmed been found on other plants, particularly on conifers such (transmission rate of 4.1%), while contradictory results as Picea abies (L.) H. Karst., Pinus sylvestris L., P.

mugo Turra, on which the new generation of adults is Molecular analyses thought to overwinter (Conci et al., 1992; Ossiannils- Individual specimens were frozen, lyophilized, ho- son, 1992; Lauterer, 1999). P. abies is the main forest mogenized, and then stored at -80 °C until their DNA species of Trentino region, covering more than one third could be extracted. Total genomic DNA was extracted of the total forest area (137203 ha out of 407500 ha) from the samples following the CTAB (cetyltrimethyl- (INFC, 2005). To date, several studies have been con- ammonium bromide) method (Doyle and Doyle, 1990). ducted on the overwintering habits of this species in To assess the presence of ‘Ca. P. mali’, all of the col- Trentino (Pedrazzoli et al., 2005; Mattedi et al., 2007). lected insects were subjected to PCR amplification of a A regular presence has been found on Norway spruce non-ribosomal DNA region of 162 bp with the specific and pine in only a few high-altitude locations (Pedraz- primers AP3/AP4 (Jarausch et al., 1994). The PCR as- zoli et al., 2005). says were performed with 100-150 ng DNA, 375 nM of The different roles assigned to C. melanoneura by the each primer and the 2x Go Taq® Green Master Mix studies conducted to date suggest the existence of dif- (Promega, Madison, USA), in a final reaction volume of ferent populations, characterized by a different level of 20 µl. The PCR parameters were as follows: an initial infectivity. To examine these differences thoroughly, denaturation of 2 min at 95 °C and 40 cycles with 30 sec molecular analyses were performed on overwintered C. at 95 °C, 30 sec at 57 °C, 30 sec at 72 °C and a final ex- melanoneura collected from different plant species (ap- tension of 5 min at 72 °C. Amplifications were per- ple, hawthorn and conifers) in several areas of Italy. formed in a Gene Amp® PCR System 9700 (Applied Hawthorn hedgerows are a common component of the Biosystems, Foster City, CA, USA). The total DNA ex- rural landscape of Trentino region, so that often they are tracted from infected insects and a reaction blank (Milli- close to apple orchards. The knowledge of the infectiv- Q water) were included in the experiments as controls. ity of C. melanoneura collected from hawthorn plants PCR products were analyzed by electrophoresis on 1.5% could be informative about alternative inoculum w/v agarose gels stained with SYBR® Safe DNA gel sources. stain (Invitrogen, Carlsbad, CA, USA) and visualized In the present work, we report the results of these in- under UV light with the Gel Doc XR System molecular vestigations, underlining the correlation between the in- imager (BIO-RAD, Hercules, CA, USA; figure 1). fection level in the different plants and in the insects. Data analysis The correlation between the proportion of infected in- Materials and methods sects and the presence of symptomatic plants in apple or- chards was analysed applying the median test for the cor- collection relation between two variables proposed by Blomqvist The research was conducted in the Trentino and Ve- (1950). As there is not an official classification of the neto regions (northeastern Italy) and in the Aosta Valley level of infected orchards, we did an arbitrary classifica- (northwestern Italy) between 2005 and 2007, as reported tion dividing apple orchards in four classes: low (with a in table 1. Overwintering adults of C. melanoneura were percentage of symptomatic plants ranging from 0 to 10), collected from apple trees and hawthorn bushes at the middle (from 10% to 30% of symptomatic plants), high end of March and from conifers during December and (from 30% to 50%) and very high (more than 50%). This January, using the beat tray method. The specimens analysis was not carried out for the other plant species, as were identified using Ossiannilsson’s keys (1992). no symptoms were detected on hawthorn and conifers.

Table 1. Samples of C. melanoneura populations collected from different host plants in different locations. The to- tal number of psyllids analysed, the proportion of AP-infected samples and infection level in the sampled orchards are given.

Insects Infection level in the Host plant Locality Location infected/tot. percentage sampled orchards Apple Borgo (Trentino) 46°3'N 11°29'E 11/96 11.46% very high " Oltrecastello (Trentino) 46°4'N 11°9'E 27/113 23.87% high " S. Michele (Trentino) 46°11'N 11°8'E 5/96 5.14% middle " Vervò (Trentino) 46°18'N 11°7'E 3/90 3.33% middle " Vigalzano (Trentino) 46°4'N 11°14'E 10/96 10.42% high " Aosta (Aosta Valley) 45°44'N 7°18'E 11/59 18.63% very high " Schio (Veneto) 45°42'N 11°24'E 0/12 0% low " Verona (Veneto) 45°39'N 10°53'E 0/15 0% low Hawthorn Cles (Trentino) 46°21'N 11°2'E 2/96 2.08% - " Mezzolombardo (Trentino) 46°11'N 11°6'E 2/63 3.17% - " Rumo (Trentino) 46°26'N 11°1'E 0/44 0% - " Chambave (Aosta Valley) 45°44'N 7°33'E 8/53 15.10% - Conifers Sopramonte (Trentino) 46°4'N 11°4'E 4/49 8.16% - " Vason (Trentino) 46°2'N 11°3'E 5/38 13.15% -

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←162 bp

Ld 1 2 3 4 5 6 7 8 9 10 11 Ld

Figure 1. Agarose gel electrophoresis of PCR amplifications with primer pair AP3/AP4. Ld = molecular size marker (100 bp DNA Ladder, New England Biolabs, Inc., Beverly, MA, USA); 1-2 = positive controls (infected psyllids); 3 = negative control (water); 4-5-6 = psyllids collected from hawthorn; 7-8-9 = psyllids collected from apple plants; 10-11 = psyllids collected from Norway spruce. A 162 bp fragment is the expected amplification product, while the lower bands in some of the lanes are primer dimers, which are present especially in negative or weakly positive samples.

Results but nobody has ever tested this hypothesis. In this re- search we detected for the first time ‘Ca. P. mali’ in in- The results of PCR amplifications performed on the dif- dividuals collected from conifers during the winter. As ferent C. melanoneura populations are reported in table 1, these host plants have never been found infected by ‘Ca. where the percentages of infected individuals and the P. mali’ (unpublished data), it is reliable that these indi- mean infection levels of the apple trees are listed for viduals had acquired the phytoplasma before overwin- each population. A total number of 920 insects belong- tering. These results are consistent with the behaviour of ing to 14 different localities (10 located in Trentino, two other psyllid vectors of phytoplasma, such as C. pyri- in Aosta Valley and two in Veneto) were analysed. cola and C. pyri which may retain infectivity during the Regarding populations collected from apple in Tren- winter season (Davies et al., 1998; Carraro et al., 2001a; tino, data showed differences in the percentage of ‘Ca. Thébaud et al., 2009). Therefore, some overwintering C. P. mali’-infected psyllids, which ranged from 3% melanoneura adults are already infected, even in high (Vervò) to 24% (Oltrecastello) (table 1). Few infected percentages, with the phytoplasma when they come psyllids were found among populations collected from back to the apple orchards. The high mean percentage of hawthorn and none of the examined hawthorn hedge- infected insects collected on conifers could depend on rows ever showed disease symptoms or tested positive the restricted number of samples analysed. A wider for the presence of the pathogen (unpublished data). A sampling activity on conifers is needed to confirm these relatively large number of positive insects were col- data and to obtain more consistent values. lected in the Aosta Valley, from both apple (18.63%) Moreover, psyllids can acquire ‘Ca. P. mali’ after a and hawthorn (15.10%). The percentage of infected period of feeding on infected trees. Psyllids were col- psyllids of Aosta Valley was higher than that of Tren- lected in the Trentino region at the peak of overwinter- tino region for both hawthorn and apple, with the only ing adults, when the population densities are the highest, exception of the apple population from Oltrecastello. PCR amplification revealed no infected insects among the psyllids collected in two different areas in the Ve- 25 neto region. Eight to 13% of the psyllids collected from conifers in northeastern Italy were tested positive for 20 ‘Ca. P. mali’ (table 1). A positive correlation was found with the Blomqvist 15 median test (1950) between the proportion of infected 10 psyllids and the infection level of the apple orchards where captures took place (P = 0.0143; figure 2). %of infected insects 5

0

01234 Discussion Class

The present work provides evidence that the overwinter- Figure 2. Scatter diagram of the observed infection per- ing populations of C. melanoneura in northern Italy can centage in the insect populations and the correspond- carry ‘Ca. P. mali’, since the PCR analyses revealed the ing infection level in the orchards (1 = low infection, 2 presence of infected psyllids. Tedeschi et al. (2003, = middle infection, 3 = high infection, 4 = very high 2006) already suggested the possibility that the phyto- infection). The broken lines indicate the sample medi- plasma overwinters in the bodies of this insect vector, ans of the values.

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so that they had spent a few weeks of feeding on highly The infection rates observed in this survey for the infected apple trees. A period of four days is sufficient populations collected from apple and hawthorn in Aosta for C. melanoneura to acquire AP phytoplasma Valley are higher than those previously reported for the (Pedrazzoli et al., 2007). At the end of March, when same region (Tedeschi et al. 2003; 2009; Tedeschi and captures took place, ‘Ca. P. mali’ is present in the aerial Alma, 2007). These different data could reflect the use part of apple trees with an uneven distribution which in of different primers (AP3/AP4 vs. P1/P7, followed by some cases reaches high concentration levels (Pedraz- nested PCR with fO1/rO1 primers) in the molecular zoli et al., 2008a). The percentages of infected psyllids analyses and/or the different number of psyllids ana- are variable among Trentino populations collected from lyzed (Tedeschi et al., 2003; Tedeschi and Alma, 2007), apple; the mean proportion of ‘Ca. P. mali’-positive in- the size of the sampled populations or the period of col- sects (10.84%) in overwintering psyllids collected in lection and the infection levels of the plants. 2006 on apple was comparable to the rates already re- The results obtained in this work suggest the presence ported for overwintering C. melanoneura adults in this of a high variability in the infection level within the region (Pedrazzoli et al., 2008b). The highest infection different populations of C. melanoneura in northern levels for Trentino populations are comparable to that of Italy and even within the Trentino region. These differ- Aosta Valley population. In both cases, psyllids were ences could depend on the affinity between the phyto- collected in orchards with high percentages of sympto- plasma and the insects, due to the presence of various matic apple trees. On the other hand, lower infection ‘Ca. P. mali’ strains (AT-2 is predominant in Trentino, rates were detected in populations collected in low while AT-1 is more widespread in Aosta Valley), or to symptomatic plantations; moreover, in the Veneto re- the characteristics of the psyllid populations (Cainelli, gion there was no evidence of infected psyllids, but 2007; Malagnini et al., 2008). Furthermore, the differ- there were also few AP-symptomatic apple trees. ences in the natural infection rates could explain Goodwin et al. (1999) found out that the presence of the differences observed in previous transmission trials infected Macrosteles quadrilineatus (Forbes) individu- carried out in Aosta Valley and Trentino regions als is a better predictor of aster yellows infection in let- (Tedeschi and Alma, 2004; Mattedi et al., 2005; 2007; tuce fields than the total number of leafhoppers and the 2008). This hypothesis is also supported by data ob- quantity of phytoplasmas in the vector insects. There- tained in Germany where C. melanoneura never trans- fore, the positive correlation between the infection rates mitted ‘Ca. P. mali’ (Jarausch W. et al., 2004, Mayer et in plants and psyllids, which was confirmed by the sta- al., 2009); in this region overwintering adults of C. tistical analysis performed in this work, could be a use- melanoneura collected in apple orchards show a very ful tool in the disease management. For instance, within low infection rate (Jarausch et al., 2008; Mayer et al., the phytosanitary measures adopted to reduce the inocu- 2009). Further studies of transmission efficiency should lum source, such as uprooting diseased plants, the num- take into account these differences among populations ber of infected psyllids should be taken into account as a of C. melanoneura. predictor of latent infections in an orchard together with the presence of symptoms in the plants. Regarding the infection level among the psyllids col- Acknowledgements lected from hawthorn, the percentages obtained for the Trentino region (mean value 1.75%) are lower than that The authors thank Dr. R. Tedeschi (University of Turin, for the Aosta Valley (15.1%). The proportions of in- Italy) and the Phytosanitary Service of the Veneto Re- fected psyllids reported in this study for populations gion (Italy) for the insects; Dr. V. Mazzoni for his sug- from Aosta Valley are similar in individuals collected gestions (FEM-IASMA, Italy). This research was fi- from both hosts (apple and hawthorn). This result is con- nanced by the Province of Trento (Italy). sistent with preliminary ecological observations carried out in north-western Italy, indicating that the populations of C. melanoneura collected from apple can survive and References reproduce also on hawthorn, while C. melanoneura col- lected from hawthorn seems to be more selective (R. BLOMQVIST N., 1950.- On a measure of dependence between Tedeschi, personal communication). A certain exchange two random variables.- The Annals of Mathematical Statis- in the populations could therefore take place, resulting in tics, 21: 593-600. a more homogeneous infection level in the insects. In CAINELLI C., 2007.- Population dynamics of apple prolifera- Trentino region, apple orchards are often close to stands tion in Trentino. 171 pp. Ph.D. Thesis, Università degli Stu- so that C. melanoneura populations are sympatric. How- di di Verona, Italy. CARRARO L., LOI N., EMARCORA P., 2001a.- The ‘life cycle’ of ever, they seem more linked to their original host, show- pear decline phytoplasma in the vector Cacospylla pyri.- ing a significantly reduced fitness when moved onto the Journal of Plant Pathology, 83: 87-90. alternative host plant (Malagnini et al., unpublished CARRARO L., OSLER R., LOI N., ERMACORA P., REFATTI E., data). High populations of C. melanoneura were re- 2001b.- Fruit tree phytoplasma diseases diffused in nature corded on hawthorn, while no psyllids were observed in by psyllids.- Acta Horticulturae, 550: 345-350. the close apple orchard (unpublished data). This could CONCI C., RAPISARDA C., TAMANINI L., 1992.- Annotated cata- also lead to different percentages of infected individuals logue of the Italian . First Part (Insecta Homop- for the two plant species in this region, even though the tera).- Atti Accademia Roveretana degli Agiati, 242 (2B): two plant species are close to each other. 33-135.

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TEDESCHI R., FERRATO V., ROSSI J., ALMA A., 2006.- Possible MATTEDI L., FORNO F., VARNER M., 2007.- Scopazzi del melo, phytoplasma transovarian transmission in the psyllids Cacop- p. 144. In: Conoscenze ed osservazioni di campo.- Arti Gra- sylla melanoneura and Cacopsylla pruni.- Plant Pathology, 55: fiche La Commerciale, Borgogno, Bolzano, Italy. 18-24. MATTEDI L., FORNO F., CAINELLI C., GRANDO M. S., JARAUSCH TEDESCHI R., LAUTERER P., BRUSETTI L., TOTA F., ALMA A., W., 2008.- Research on Candidatus Phytoplasma mali 2009.- Composition, abundance and phytoplasma infection transmission by insect vectors in Trentino.- Acta Horticul- in the hawthorn psyllid fauna of northwestern Italy.- Euro- turae, 781: 369-374. pean Journal of Plant Pathology, 123: 301-310. MAYER C. J., JARAUSCH B., JARAUSCH W., JELKMANN W., VIL- THÉBAUD G., YVON M., ALARY R., SAUVION N., LABONNE G., CINSKAS A., GROSS J., 2009.- Cacopsylla melanoneura has 2009.- Efficient transmission of ‘Candidatus Phytoplasma no relevance as vector of apple proliferation in Germany.- prunorum’ is delayed by eight months due to a long latency Phytopathology, 99 (6): 729-738. in its host-alternating vector.- Phytopathology, 99 (3): 265- OSSIANNILSSON F., 1992.- The Psylloidea (Homoptera) of 273. Fennoscandia and Denmark, p. 346. In: Fauna Entomologi- VINDIMIAN E., DELAITI L., 1996.- Indagine sistematica sugli ca Scandinavica, vol. 26 (KRISTENSEN N. P., MICHELSEN V., scopazzi del melo.- Terra trentina, 13 (11): 30-33. Eds).- E.J. Brill, Leiden, The Netherlands. Authors’ addresses: Valeria MALAGNINI, (corresponding PEDRAZZOLI F., FORNO F., MALAGNINI V., MATTEDI L., 2005.- author: [email protected]), Federico PEDRAZZOLI, Indagini bioecologiche su Cacopsylla melanoneura (Förster) Valeria GUALANDRI, Rosaly ZASSO, Elisa BOZZA, Federica (Homoptera: Psyllidae), p. 251. In: Proceedings XX Con- FIAMINGO, Claudio IORIATTI, Centro Trasferimento Tecnolo- gresso Nazionale Italiano di Entomologia, Perugia, Assisi, gico, FEM-IASMA, via E. Mach 1, 38010 S. Michele Italy, 13-18 June 2005. all’Adige, Trento, Italy; Alberto POZZEBON, Nicola MORI, De- PEDRAZZOLI F., GUALANDRI V., FORNO F., MATTEDI L., MA- partment of Environmental Agronomy and Crop Science, LAGNINI V., SALVADORI A., STOPPA G., IORIATTI C., 2007.- University of Padua, viale dell’Università 16, 35020 Legnaro, Acquisition capacities of the overwintering adults of the psyllid Padova, Italy. vectors of ‘Candidatus Phytoplasma mali’.- Bulletin of Insec- tology, 60 (2): 195-196. Received July 30, 2009. Accepted December 1, 2009.

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